Regulation of chloroplast protein degradation

Yang Sun; Jialong Li; Lixin Zhang; Rongcheng Lin

doi:10.1016/j.jgg.2023.02.010

Volume 50 Issue 6

Jun. 2023

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Article Navigation > Journal of Genetics and Genomics > 2023 > 50(6): 375-384

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Regulation of chloroplast protein degradation

doi: 10.1016/j.jgg.2023.02.010

a. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, Henan 475001, China;
b. Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

Funds:

D Program of China (2020YFA0907600).

This work was supported by grant from the National Key R&

Received Date: 2022-12-24
Accepted Date: 2023-02-14
Rev Recd Date: 2023-02-02
Publish Date: 2023-02-28

Abstract

Abstract

Chloroplasts are unique organelles that not only provide sites for photosynthesis and many metabolic processes, but also are sensitive to various environmental stresses. Chloroplast proteins are encoded by genes from both nuclear and chloroplast genomes. During chloroplast development and responses to stresses, the robust protein quality control systems are essential for regulation of protein homeostasis and the integrity of chloroplast proteome. In this review, we summarize the regulatory mechanisms of chloroplast protein degradation refer to protease system, ubiquitin-proteasome system, and the chloroplast autophagy. These mechanisms symbiotically play a vital role in chloroplast development and photosynthesis under both normal or stress conditions.
- Chloroplast,
- Protein homeostasis,
- Protease,
- Ubiquitin-proteasome,
- Chlorophagy

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References(124)

References

[1]	Apitz, J., Nishimura, K., Schmied, J., Wolf, A., Hedtke, B., van Wijk, K.J., Grimm, B., 2016. Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol. 170, 2040-2051.
[2]	Bouchnak, I., van Wijk, K.J., 2019. N-Degron pathways in plastids. Trends Plant Sci. 24, 917-926.
[3]	Bouchnak, I., van Wijk, K.J., 2021. Structure, function, and substrates of Clp AAA+ protease systems in cyanobacteria, plastids, and apicoplasts: a comparative analysis. J. Biol. Chem. 296, 100338.
[4]	Bujaldon, S., Kodama, N., Rappaport, F., Subramanyam, R., de Vitry, C., Takahashi, Y., Wollman, F.A., 2017. Functional accumulation of antenna proteins in chlorophyll b-less mutants of Chlamydomonas reinhardtii. Mol. Plant 10, 115-130.
[5]	Butenko, Y., Lin, A., Naveh, L., Kupervaser, M., Levin, Y., Reich, Z., Adam, Z., 2018. Differential roles of the thylakoid lumenal Deg protease homologs in chloroplast proteostasis. Plant Physiol. 178, 1065-1080.
[6]	Chassin, Y., Kapri-Pardes, E., Sinvany, G., Arad, T., Adam, Z., 2002. Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol. 130, 857-864.
[7]	Chen, J., Burke, J.J., Xin, Z., 2018. Chlorophyll fluorescence analysis revealed essential roles of FtsH11 protease in regulation of the adaptive responses of photosynthetic systems to high temperature. BMC Plant Biol. 18, 11.
[8]	Chi, W., Sun, X., Zhang, L., 2012. The roles of chloroplast proteases in the biogenesis and maintenance of photosystem II. Biochim. Biophys. Acta 1817, 239-246.
[9]	Chiba, A., Ishida, H., Nishizawa, N.K., Makino, A., Mae, T., 2003. Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol. 44, 914-921.
[10]	Clausen, T., Kaiser, M., Huber, R., Ehrmann, M., 2011. HTRA proteases: regulated proteolysis in protein quality control. Nat. Rev. Mol. Cell Biol. 12, 152-162.
[11]	D'Andrea, L., Simon-Moya, M., Llorente, B., Llamas, E., Marro, M., Loza-Alvarez, P., Li, L., Rodriguez-Concepcion, M., 2018. Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening. J. Exp. Bot. 69, 1557-1568.
[12]	Daras, G., Rigas, S., Tsitsekian, D., Zur, H., Tuller, T., Hatzopoulos, P., 2014. Alternative transcription initiation and the AUG context configuration control dual-organellar targeting and functional competence of Arabidopsis Lon1 protease. Mol. Plant 7, 989-1005.
[13]	Day, P.M., Theg, S.M., 2018. Evolution of protein transport to the chloroplast envelope membranes. Photosynth. Res. 138, 315-326.
[14]	Deshaies, R.J., Joazeiro, C.A.P., 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
[15]	Ding, X., Zhang, X., Otegui, M.S., 2018. Plant autophagy: new flavors on the menu. Curr. Opin. Plant Biol. 46, 113-121.
[16]	Dogra, V., Singh, R.M., Li, M., Li, M., Singh, S., Kim, C., 2022. EXECUTER2 modulates the EXECUTER1 signalosome through its singlet oxygen-dependent oxidation. Mol. Plant 15, 438-453.
[17]	Dominguez, F., Cejudo, F.J., 2021. Chloroplast dismantling in leaf senescence. J. Exp. Bot. 72, 5905-5918.
[18]	Enam, C., Geffen, Y., Ravid, T., Gardner, R.G., 2018. Protein quality control degradation in the nucleus. Annu. Rev. Biochem. 87, 725-749.
[19]	Flores-Perez, U., Bedard, J., Tanabe, N., Lymperopoulos, P., Clarke, A.K., Jarvis, P., 2016. Functional analysis of the Hsp93/ClpC chaperone at the chloroplast envelope. Plant Physiol. 170, 147-162.
[20]	Frank, S., Hollmann, J., Mulisch, M., Matros, A., Carrion, C.C., Mock, H.P., Hensel, G., Krupinska, K., 2019. Barley cysteine protease PAP14 plays a role in degradation of chloroplast proteins. J. Exp. Bot. 70, 6057-6069.
[21]	Fu, W., Cui, Z., Guo, J., Cui, X., Han, G., Zhu, Y., Hu, J., Gao, X., Li, Y., Xu, M., et al., 2023. Immunophilin CYN28 is required for accumulation of photosystem II and thylakoid FtsH protease in Chlamydomonas. Plant Physiol. 191, 1002-1016.
[22]	Fu, Y., Li, X., Fan, B., Zhu, C., Chen, Z., 2022. Chloroplasts protein quality control and turnover: a multitude of mechanisms. Int. J. Mol. Sci. 23, 7760.
[23]	Galluzzi, L., Baehrecke, E.H., Ballabio, A., Boya, P., Bravo-San Pedro, J.M., Cecconi, F., Choi, A.M., Chu, C.T., Codogno, P., Colombo, M.I., et al., 2017. Molecular definitions of autophagy and related processes. EMBO J. 36, 1811-1836.
[24]	Grimmer, J., Helm, S., Dobritzsch, D., Hause, G., Shema, G., Zahedi, R.P., Baginsky, S., 2020. Mild proteasomal stress improves photosynthetic performance in Arabidopsis chloroplasts. Nat. Commun. 11, 1662.
[25]	Hatfield, P.M., Gosink, M.M., Carpenter, T.B., Vierstra, R.D., 1997. The ubiquitin-activating enzyme (E1) gene family in Arabidopsis thaliana. Plant J. 11, 213-226.
[26]	Honig, A., Avin-Wittenberg, T., Ufaz, S., Galili, G., 2012. A new type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 24, 288-303.
[27]	Huang, W., Chen, Q., Zhu, Y., Hu, F., Zhang, L., Ma, Z., He, Z., Huang, J., 2013. Arabidopsis thylakoid formation 1 is a critical regulator for dynamics of PSII-LHCII complexes in leaf senescence and excess light. Mol. Plant 6, 1673-1691.
[28]	Huesgen, P.F., Schuhmann, H., Adamska, I., 2006. Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett. 580, 6929-6932.
[29]	Huesgen, P.F., Schuhmann, H., Adamska, I., 2009. Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Res. Microbiol. 160, 726-732.
[30]	Inagaki, N., 2022. Processing of D1 protein: a mysterious process carried out in thylakoid lumen. Int. J. Mol. Sci. 23, 2520.
[31]	Ishida, H., Izumi, M., Wada, S., Makino, A., 2014. Roles of autophagy in chloroplast recycling. Biochim. Biophys. Acta 1837, 512-521.
[32]	Ishida, H., Yoshimoto, K., Izumi, M., Reisen, D., Yano, Y., Makino, A., Ohsumi, Y., Hanson, M.R., Mae, T., 2008. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 148, 142-155.
[33]	Izumi, M., Ishida, H., 2019. An additional role for chloroplast proteins-an amino acid reservoir for energy production during sugar starvation. Plant Signal. Behav. 14, 1552057.
[34]	Izumi, M., Ishida, H., Nakamura, S., Hidema, J., 2017. Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29, 377-394.
[35]	Izumi, M., Nakamura, S., Li, N., 2019. Autophagic turnover of chloroplasts: its roles and regulatory mechanisms in response to sugar starvation. Front. Plant Sci. 10, 280.
[36]	Izumi, M., Wada, S., Makino, A., Ishida, H., 2010. The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol. 154, 1196-1209.
[37]	Jarvi, S., Suorsa, M., Tadini, L., Ivanauskaite, A., Rantala, S., Allahverdiyeva, Y., Leister, D., Aro, E.M., 2016. Thylakoid-bound FtsH proteins facilitate proper biosynthesis of photosystem I. Plant Physiol. 171, 1333-1343.
[38]	Jarvis, P., Lopez-Juez, E., 2013. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14, 787-802.
[39]	Johansen T., Lamark T., 2020. Selective autophagy: ATG8 family proteins, LIR motifs and cargo receptors. J. Mol. Biol. 432, 80-103.
[40]	Kato, Y., Miura, E., Ido, K., Ifuku, K., Sakamoto, W., 2009. The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol. 151, 1790-1801.
[41]	Kato, Y., Sakamoto, W., 2014. Phosphorylation of photosystem II core proteins prevents undesirable cleavage of D1 and contributes to the fine-tuned repair of photosystem II. Plant J. 79, 312-321.
[42]	Kato, Y., Sakamoto, W., 2018. FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. Front. Plant Sci. 9, 855.
[43]	Kikuchi, S., Asakura, Y., Imai, M., Nakahira, Y., Kotani, Y., Hashiguchi, Y., Nakai, Y., Takafuji, K., Bedard, J., Hirabayashi-Ishioka, Y., et al., 2018. A Ycf2-FtsHi heteromeric AAA-ATPase complex is required for chloroplast protein import. Plant Cell 30, 2677-2703.
[44]	Kikuchi, Y., Nakamura, S., Woodson, J.D., Ishida, H., Ling, Q., Hidema, J., Jarvis, R.P., Hagihara, S., Izumi, M., 2020. Chloroplast autophagy and ubiquitination combine to manage oxidative damage and starvation responses. Plant Physiol. 183, 1531-1544.
[45]	Kim, J., Kimber, M.S., Nishimura, K., Friso, G., Schultz, L., Ponnala, L., van Wijk, K.J., 2015. Structures, functions, and interactions of ClpT1 and ClpT2 in the Clp protease system of Arabidopsis chloroplasts. Plant Cell 27, 1477-1496.
[46]	Kim, D.Y., Scalf, M., Smith, L.M., Vierstra, R.D., 2013. Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell. 25, 1523-1540.
[47]	Kirchhoff, H., 2019. Chloroplast ultrastructure in plants. New Phytol. 223, 565-574.
[48]	Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.S., Deng, X.W., Callis, J., 2005. Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139, 1597-1611.
[49]	Krieger-Liszkay, A., Krupinska, K., Shimakawa, G., 2019. The impact of photosynthesis on initiation of leaf senescence. Physiol. Plantarum 166, 148-164.
[50]	Krynicka, V., Skotnicova, P., Jackson, P.J., Barnett, S., Yu, J., Wysocka, A., Kana, R., Dickman, M.J., Nixon, P.J., Hunter, C.N., Komenda, J., 2023. FtsH4 protease controls biogenesis of the PSII complex by dual regulation of high light-inducible proteins. Plant Commun. 4, 100502.
[51]	Kuhlmann, N.J., Chien, P., 2017. Selective adaptor dependent protein degradation in bacteria. Curr. Opin. Microbiol. 36, 118-127.
[52]	Lee, D.W., Kim, S.J., Oh, Y.J., Choi, B., Lee, J., Hwang, I., 2016. Arabidopsis BAG1 functions as a cofactor in Hsc70-mediated proteasomal degradation of unimported plastid proteins. Mol. Plant 9, 1428-1431.
[53]	Li, J., Yuan, J., Li, Y., Sun, H., Ma, T., Huai, J., Yang, W., Zhang, W., Lin, R., 2022. The CDC48 complex mediates ubiquitin-dependent degradation of intra-chloroplast proteins in plants. Cell Rep. 39, 110664.
[54]	Li, L., Nelson, C., Fenske, R., Trosch, J., Pruzinska, A., Millar, A.H., Huang, S., 2017. Changes in specific protein degradation rates in Arabidopsis thaliana reveal multiple roles of Lon1 in mitochondrial protein homeostasis. Plant J. 89, 458-471.
[55]	Lee, Sookjin, Lee, D.W., Lee, Y., Mayer, U., Stierhof, Y.D., Lee, Sumin, Jurgens, G., Hwang, I., 2010. Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21, 3984-4001.
[56]	Li, X., Mu, Y., Sun, X., Zhang, L., 2010. Increased sensitivity to drought stress in atlon4 Arabidopsis mutant. Chin. Sci. Bull. 55, 3668-3672.
[57]	Ling, Q., Broad, W., Trosch, R., Topel, M., Demiral Sert, T., Lymperopoulos, P., Baldwin, A., Jarvis, R.P., 2019. Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science 363, eaav4467.
[58]	Ling, Q., Huang, W., Baldwin, A., Jarvis, P., 2012. Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338, 655-659.
[59]	Ling, Q., Jarvis, P., 2015. Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants. Curr. Biol. 25, 2527-2534.
[60]	Linster, E., Wirtz, M., 2018. N-terminal acetylation: an essential protein modification emerges as an important regulator of stress responses. J. Exp. Bot. 69, 4555-4568.
[61]	Llamas, E., Pulido, P., 2022. A proteostasis network safeguards the chloroplast proteome. Essays Biochem. 66, 219-228.
[62]	Lucinski, R., Misztal, L., Samardakiewicz, S., Jackowski, G., 2011a. Involvement of Deg5 protease in wounding-related disposal of PsbF apoprotein. Plant Physiol. Biochem. 49, 311-320.
[63]	Lucinski, R., Misztal, L., Samardakiewicz, S., Jackowski, G., 2011b. The thylakoid protease Deg2 is involved in stress-related degradation of the photosystem II light-harvesting protein Lhcb6 in Arabidopsis thaliana. New Phytol. 192, 74-86.
[64]	Malnoe, A., Wang, F., Girard-Bascou, J., Wollman, F.A., de Vitry, C., 2014. Thylakoid FtsH protease contributes to photosystem II and cytochrome b6f remodeling in Chlamydomonas reinhardtii under stress conditions. Plant Cell 26, 373-390.
[65]	Mamaeva, A., Taliansky, M., Filippova, A., Love, A.J., Golub, N., Fesenko, I., 2020. The role of chloroplast protein remodeling in stress responses and shaping of the plant peptidome. New Phytol. 227, 1326-1334.
[66]	Marshall, R.S., Vierstra, R.D., 2018. Autophagy: the master of bulk and selective recycling. Annu. Rev. Plant Biol. 69, 173-208.
[67]	Mechela, A., Schwenkert, S., Soll, J., 2019. A brief history of thylakoid biogenesis. Open Biol. 9, 180237.
[68]	Michaeli, S., Honig, A., Levanony, H., Peled-Zehavi, H., Galili, G., 2014. Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26, 4084–4101.
[69]	Mishra, L.S., Funk, C., 2021. The FtsHi enzymes of Arabidopsis thaliana: pseudo-proteases with an important function. Int. J. Mol. Sci. 22, 5917.
[70]	Nakamura, S., Hidema, J., Sakamoto, W., Ishida, H., Izumi, M., 2018. Selective elimination of membrane-damaged chloroplasts via microautophagy. Plant Physiol. 177, 1007-1026.
[71]	Ng, M.Y.W., Wai, T., Simonsen, A., 2021. Quality control of the mitochondrion. Dev. Cell 56, 881-905.
[72]	Nishimura, K., Apitz, J., Friso, G., Kim, J., Ponnala, L., Grimm, B., van Wijk, K.J., 2015. Discovery of a unique Clp component, ClpF, in chloroplasts: a proposed binary ClpF-ClpS1 adaptor complex functions in substrate recognition and delivery. Plant Cell 27, 2677-2691.
[73]	Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., van Wijk, K.J., 2013. ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25, 2276-2301.
[74]	Nishimura, K., Kato, Y., Sakamoto, W., 2016. Chloroplast proteases: updates on proteolysis within and across suborganellar compartments. Plant Physiol. 171, 2280-2293.
[75]	Nishimura, K., Kato, Y., Sakamoto, W., 2017. Essentials of proteolytic machineries in chloroplasts. Mol. Plant 10, 4-19.
[76]	Olinares, P.D., Kim, J., Davis, J.I., van Wijk, K.J., 2011. Subunit stoichiometry, evolution, and functional implications of an asymmetric plant plastid ClpP/R protease complex in Arabidopsis. Plant Cell 23, 2348-2361.
[77]	Ono, Y., Wada, S., Izumi, M., Makino, A., Ishida, H., 2013. Evidence for contribution of autophagy to rubisco degradation during leaf senescence in Arabidopsis thaliana: rubisco degradation by autophagy during senescence. Plant Cell Environ. 36, 1147-1159.
[78]	Pogson, B.J., Ganguly, D., Albrecht-Borth, V., 2015. Insights into chloroplast biogenesis and development. Biochim. Biophys. Acta 1847, 1017-1024.
[79]	Pulido, P., Llamas, E., Llorente, B., Ventura, S., Wright, L.P., Rodriguez-Concepcion, M., 2016. Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding or degradation by the stromal Clp protease in Arabidopsis. PLoS Genet. 12, e1005824.
[80]	Pulido, P., Toledo-Ortiz, G., Phillips, M.A., Wright, L.P., Rodriguez-Concepcion, M., 2013. Arabidopsis J-protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25, 4183-4194.
[81]	Rigas, S., Daras, G., Tsitsekian, D., Alatzas, A., Hatzopoulos, P., 2014. Evolution and significance of the Lon gene family in Arabidopsis organelle biogenesis and energy metabolism. Front. Plant Sci. 5, 145.
[82]	Rigas, S., Daras, G., Tsitsekian, D., Hatzopoulos, P., 2012. The multifaceted role of Lon proteolysis in seedling establishment and maintenance of plant organelle function: living from protein destruction. Physiol. Plantarum 145, 215-223.
[83]	Roberts, I.N., Caputo, C., Criado, M.V., Funk, C., 2012. Senescence-associated proteases in plants. Physiol. Plantarum 145, 130-139.
[84]	Rochaix, J., 2022. Chloroplast protein import machinery and quality control. FEBS J. 289, 6908-6918.
[85]	Rodriguez-Concepcion, M., D'Andrea, L., Pulido, P., 2019. Control of plastidial metabolism by the Clp protease complex. J. Exp. Bot. 70, 2049-2058.
[86]	Sako, K., Yanagawa, Y., Kanai, T., Sato, T., Seki, M., Fujiwara, M., Fukao, Y., Yamaguchi, J., 2014. Proteomic analysis of the 26S proteasome reveals its direct interaction with transit peptides of plastid protein precursors for their degradation. J. Proteome Res. 13, 3223-3230.
[87]	Sakuraba, Y., Tanaka, R., Yamasato, A., Tanaka, A., 2009. Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J. Biol. Chem. 284, 36689-36699.
[88]	Schuhmann, H., Adamska, I., 2012. Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. Physiol. Plantarum 145, 224-234.
[89]	Schuhmann, H., Mogg, U., Adamska, I., 2011. A new principle of oligomerization of plant DEG7 protease based on interactions of degenerated protease domains. Biochem. J. 435, 167-174.
[90]	Sedaghatmehr, M., Mueller-Roeber, B., Balazadeh, S., 2016. The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis. Nat. Commun. 7, 12439.
[91]	Sedaghatmehr, M., Stuwe, B., Mueller-Roeber, B., Balazadeh, S., 2022. Heat shock factor HSFA2 fine-tunes resetting of thermomemory via plastidic metalloprotease FtsH6. J. Exp. Bot. 73, 6394-6404.
[92]	Shanmugabalaji, V., Chahtane, H., Accossato, S., Rahire, M., Gouzerh, G., Lopez-Molina, L., Kessler, F., 2018. Chloroplast biogenesis controlled by DELLA-TOC159 interaction in early plant development. Curr. Biol. 28, 2616-2623.e5.
[93]	Shen, G., Adam, Z., and Zhang, H., 2007a. The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant J. 52, 309-321.
[94]	Shen, G., Yan, J., Pasapula, V., Luo, J., He, C., Clarke, A.K., and Zhang, H., 2007b. The chloroplast protease subunit ClpP4 is a substrate of the E3 ligase AtCHIP and plays an important role in chloroplast function. Plant J. 49, 228-237.
[95]	Shi Y, Ke X, Yang X, Liu Y, Hou X., 2022. Plants response to light stress. J. Genet. Genomics. 49, 735-747.
[96]	Sjogren, L.L.E., Tanabe, N., Lymperopoulos, P., Khan, N.Z., Rodermel, S.R., Aronsson, H., Clarke, A.K., 2014. Quantitative analysis of the chloroplast molecular chaperone ClpC/Hsp93 in Arabidopsis reveals new insights into its localization, interaction with the Clp proteolytic core, and functional importance. J. Biol. Chem. 289, 11318-11330.
[97]	Song, Y., Feng, L., Alyafei, M.A.M., Jaleel, A., Ren, M., 2021. Function of chloroplasts in plant stress responses. Int. J. Mol. Sci. 22, 13464.
[98]	Spitzer, C., Li, F., Buono, R., Roschzttardtz, H., Chung, T., Zhang, M., Osteryoung, K.W., Vierstra, R.D., Otegui, M.S., 2015. The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 27, 391-402.
[99]	Sun, J.L., Li, J.Y., Wang, M.J., Song, Z.T., Liu, J.X., 2021. Protein quality control in plant organelles: current progress and future perspectives. Mol. Plant 14, 95-114.
[100]	Sun, R., Fan, H., Gao, F., Lin, Y., Zhang, L., Gong, W., Liu, L., 2012. Crystal structure of Arabidopsis Deg2 protein reveals an internal PDZ ligand locking the hexameric resting state. J. Biol. Chem. 287, 37564-37569.
[101]	Sun, X., Fu, T., Chen, N., Guo, J., Ma, J., Zou, M., Lu, C., Zhang, L., 2010a. The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol. 152, 1263-1273.
[102]	Sun, X., Ouyang, M., Guo, J., Ma, J., Lu, C., Adam, Z., Zhang, L., 2010b. The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J. 62, 240-249.
[103]	Sun, X., Peng, L., Guo, J., Chi, W., Ma, J., Lu, C., Zhang, L., 2007. Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19, 1347-1361.
[104]	Sun, Y., Yao, Z., Ye, Y., Fang, J., Chen, H., Lyu, Y., Broad, W., Fournier, M., Chen, G., Hu, Y., Mohammed, S., Ling, Q., Jarvis, R.P., 2022. Ubiquitin-based pathway acts inside chloroplasts to regulate photosynthesis. Sci. Adv. 18, eabq7352.
[105]	Tanaka, R., Tanaka, A., 2011. Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim. Biophys. Acta 1807, 968-976.
[106]	Tapken, W., Kim, J., Nishimura, K., van Wijk, K.J., Pilon, M., 2015. The Clp protease system is required for copper ion-dependent turnover of the PAA2/HMA8 copper transporter in chloroplasts. New Phytol. 205, 511-517.
[107]	Theis, J., Lang, J., Spaniol, B., Ferte, S., Niemeyer, J., Sommer, F., Zimmer, D., Venn, B., Mehr, S.F., Muhlhaus, T., Wollman, F.A., Schroda, M., 2019. The Chlamydomonas deg1c mutant accumulates proteins involved in high light acclimation. Plant Physiol. 181, 1480-1497.
[108]	Tsitsekian, D., Daras, G., Alatzas, A., Templalexis, D., Hatzopoulos, P., Rigas, S., 2019. Comprehensive analysis of Lon proteases in plants highlights independent gene duplication events. J. Exp. Bot. 70, 2185-2197.
[109]	van Doorn, W.G., Papini, A., 2013. Ultrastructure of autophagy in plant cells: a review. Autophagy 9, 1922-1936.
[110]	van Wijk, K.J., 2015. Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol. 66, 75-111.
[111]	Vierstra, R.D., 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397.
[112]	Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., Makino, A., 2009. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 149, 885-893.
[113]	Wang, L., Kim, C., Xu, X., Piskurewicz, U., Dogra, V., Singh, S., Mahler, H., Apel, K., 2016. Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc. Natl. Acad. Sci. U. S. A 113, E3792-E3800.
[114]	Wang, Q., Sullivan, R.W., Kight, A., Henry, R.L., Huang, J., Jones, A.M., Korth, K.L., 2004. Deletion of the chloroplast-localized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol. 136, 3594-3604.
[115]	Wang, Y., Yu, B., Zhao, J., Guo, J., Li, Y., Han, S., Huang, L., Du, Y., Hong, Y., Tang, D. et al., 2013. Autophagy contributes to leaf starch degradation. Plant Cell 25, 1383-1399.
[116]	Watson, S.J., Sowden, R.G., Jarvis, P., 2018. Abiotic stress-induced chloroplast proteome remodelling: a mechanistic overview. J. Exp. Bot. 69, 2773-2781.
[117]	Welsch, R., Zhou, X., Yuan, H., Alvarez, D., Sun, T., Schlossarek, D., Yang, Y., Shen, G., Zhang, H., Rodriguez-Concepcion, M., et al., 2018. Clp Protease and OR directly control the proteostasis of phytoene synthase, the crucial enzyme for carotenoid biosynthesis in Arabidopsis. Mol. Plant 11, 149-162.
[118]	Woodson, J.D., Joens, M.S., Sinson, A.B., Gilkerson, J., Salome, P.A., Weigel, D., Fitzpatrick, J.A., Chory, J., 2015. Ubiquitin facilitates a quality-control pathway that removes damaged chloroplasts. Science 350, 450-454.
[119]	Wu, X., Rapoport, T.A., 2018. Mechanistic insights into ER-associated protein degradation. Curr. Opin. Cell Biol. 53, 22-28.
[120]	Yi, L., Liu, B., Nixon, P.J., Yu, J., Chen, F., 2022. Recent advances in understanding the structural and functional evolution of FtsH proteases. Front. Plant Sci. 13, 837528.
[121]	Young, P.G., Bartel, B., 2016. Pexophagy and peroxisomal protein turnover in plants. Biochim. Biophys. Acta 1863, 999-1005.
[122]	Yue, X., Ke, X., Shi, Y., Li, Y., Zhang, C., Wang, Y., Hou, X., 2023. Chloroplast inner envelope protein FtsH11 is involved in the adjustment of assembly of chloroplast ATP synthase under heat stress. Plant Cell Environ. 46, 850-864 .
[123]	Zhang, L., Kato, Y., Otters, S., Vothknecht, U.C., Sakamoto, W., 2012. Essential role of VIPP1 in chloroplast envelope maintenance in Arabidopsis. Plant Cell 24, 3695-3707.
[124]	Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324.